Skip to main content
Log in

The neural response to transcranial magnetic stimulation of the human motor cortex. II. Thalamocortical contributions

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Beta oscillations (15–30 Hz) constitute an important electrophysiological signal recorded in the resting state over the human precentral gyrus. The brain circuitry involved in generating the beta oscillations is not well understood but appears to involve both cortical and subcortical structures. We have shown that single pulses of transcranial magnetic stimulation (TMS) applied over the primary motor cortex consistently elicit a brief beta oscillation. Reducing the local cortical excitability using low-frequency repetitive TMS does not change the amplitude of the induced beta oscillation (Van Der Werf and Paus in Exp Brain Res DOI 10.1007/s00221-006-0551-2). Here, we investigated the possible involvement of the thalamus in the cortically expressed beta response to single-pulse TMS. We included eight patients with Parkinson’s disease who had undergone unilateral surgical lesioning of the ventrolateral nucleus of the thalamus. We administered 50 single pulses of TMS, at an intensity of 120% of resting motor threshold, over the left and right primary motor cortex and, at the same time, recorded the electroencephalogram (EEG) using a 60-electrode cap. We were able to perform analyses on seven EEG data sets and found that stimulation of the unoperated hemisphere (with thalamus) resulted in higher amplitudes of the single-trial induced beta oscillations than in the operated hemisphere (with thalamotomy). The beta oscillation obtained in response to pulses applied over the unoperated hemisphere was also higher than that obtained in healthy controls. We suggest that (1) the beta oscillatory response to pulses of TMS applied over the primary motor cortex is higher in Parkinson’s disease patients, (2) thalamotomy serves to reduce the abnormally high TMS-induced beta oscillations, and (3) the motor thalamus facilitates the cortically generated oscillation, through cortico-subcortico-cortical feedback loops.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Atkinson JD, Collins DL, Bertrand G, Peters TM, Pike GB, Sadikot AF (2002) Optimal location of thalamotomy lesions for tremor associated with Parkinson disease: a probabilistic analysis based on postoperative magnetic resonance imaging and an integrated digital atlas. J Neurosurg 96:854–866

    Article  PubMed  Google Scholar 

  • Avoli M, Gloor P, Kostopoulos G, Naquet R (1990) Generalized epilepsy. Neurobiological approaches. Birkhaüser, Boston, USA

    Google Scholar 

  • Bevan MD, Magill PJ, Terman D, Bolam JP, Wilson CJ (2002) Move to the rhythm: oscillations in the subthalamic nucleus-external globus pallidus network. Trends Neurosci 25:525–531

    Article  PubMed  CAS  Google Scholar 

  • Brown P (2003) Oscillatory nature of human basal ganglia activity: relationship to the pathophysiology of Parkinson’s Disease. Mov Disord 18:357–363

    Article  PubMed  Google Scholar 

  • Brown P, Williams D (2005) Basal ganglia local field potential activity: character and functional significance in the human. Clin Neurophysiol 116:2510–2519

    Article  PubMed  Google Scholar 

  • Brown P, Oliviero A, Mazzone P, Insola A, Tonali P, Di Lazzaro V (2001) Dopamine dependency of oscillations between subthalamic nucleus and pallidum in Parkinson’s disease. J Neurosci 21:1033–1038

    PubMed  CAS  Google Scholar 

  • Cassidy M, Mazzone P, Oliviero A, Insola A, Tonali P, Di Lazzaro V, Brown P (2002) Movement-related changes in synchronization in the human basal ganglia. Brain 125:1235–1246

    Article  PubMed  Google Scholar 

  • Colebatch JG, Dieber MP, Passingham RE, Friston KJ, Frackowiak RS (1991) Regional cerebral blood flow during voluntary arm and hand movements in human subjects. J Neurophysiol 65:1392–1401

    PubMed  CAS  Google Scholar 

  • Collins DL, Neelin P, Peters TM, Evans AC (1994) Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J Comp Assist Tomogr 18:192–205

    Article  CAS  Google Scholar 

  • Deschênes M, Veinante P, Zhang ZW (1998) The organization of corticothalamic projections: reciprocity versus parity. Brain Res Rev 28:286–308

    Article  PubMed  Google Scholar 

  • Dettmers C, Fink GR, Lemon RN, Stephan KM, Passingham RE, Silbersweig D, Holmes D, Ridding MC, Brooks DJ, Frakowiak RS (1995) Relation between cerebral activity and force in motor areas of the brain. J Neurophysiol 74:802–815

    PubMed  CAS  Google Scholar 

  • Doyle LMF, Kühn AA, Hariz M, Kupsch A, Schnieder G-H, Brown P (2005a) Levodopa-induced modulation of subthalamic beta oscillations during self-paced movements in patients with Parkinson’s disease. Eur J Neurosci 21:1403–1412

    Article  CAS  Google Scholar 

  • Doyle LMF, Yarrow K, Brown P (2005b) Lateralization of event-related beta desynchronization in the EEG during pre-cued reaction time tasks. Clin Neurophysiol 116:1879–1888

    Article  Google Scholar 

  • Duval C, Panisset M, Bertrand G, Sadikot AF (2000) Evidence that ventrolateral thalamotomy may eliminate the supraspinal component of both pathological and physiological tremors. Exp Brain Res 132:216–222

    Article  PubMed  CAS  Google Scholar 

  • Foffani G, Bianchi AM, Baselli G, Priori A (2005) Movement-related frequency modulation of beta oscillatory activity in the human subthalamic nucleus. J Physiol 568:699–711

    Article  PubMed  CAS  Google Scholar 

  • Fogelson N, Williams D, Tijssen M, Van Bruggen, Speelman H, Brown P (2006) Different functional loops between cerebral cortex and the subthalamic area in Parkinson’s disease. Cerebral Cortex 16:64–75

    Article  PubMed  Google Scholar 

  • Grafton ST, Woods RP, Mazziota JC (1993) Within-arm somatotopy in human motor areas determined by positron emission tomography imaging of cerebral blood flow. Exp Brain Res 95:172–176

    Article  PubMed  CAS  Google Scholar 

  • Hari R, Salmelin R (1997) Human cortical oscillations: a neuromagnetic view through the skull. Trends Neurosci 20:44–49

    Article  PubMed  CAS  Google Scholar 

  • Ilinsky IA, Kultas-Ilinsky K, Rosina A, Haddy M (1987) Quantitative evaluation of crossed and uncrossed projections from basal ganglia and cerebellum to the cat thalamus. Neuroscience 21:207–227

    Article  PubMed  CAS  Google Scholar 

  • Jahanshahi M, Jenkins IH, Brown RG, Marsden CD, Passingham RE, Brooks DJ (1995) Self-initiated versus externally triggered movements: I. An investigation using measurement of cerebral blood flow with PET and movement-related potentials in normal and Parkinson’s disease subjects. Brain 118:913–933

    Article  PubMed  Google Scholar 

  • Jasper HH, Andrews HL (1936) Human brain rhythms I. Recording Techniques and preliminary results. J Gen Psychol 14:98–126

    Article  Google Scholar 

  • Jasper HH, Andrews HL (1938) Electroencephalography III. Normal differentiation of occipital and precentral regions in man. Arch Neurol Psychiat 39:96–115

    Google Scholar 

  • Jasper HH, Penfield W (1949) Electrocorticograms in man: effect of voluntary movement upon the electrical activity of the precentral gyrus. Arch f Psych Zeitschr 183:163–174

    Article  Google Scholar 

  • Jenkins IH, Brooks DJ, Nixon PD, Frackowiak RS, Passingham RE (1994) Motor sequence learning: a study with positron emission tomography. J Neurosci 14:3775–3790

    PubMed  CAS  Google Scholar 

  • Kühn AA, Williams D, Kupsch A, Limousin P, Hariz M, Schneider G-H, Yarrow K, Brown P (2004) Event-related beta desynchronization in human subthalamic nucleus correlates with motor performance. Brain 127:735–746

    Article  PubMed  Google Scholar 

  • Levy R, Ashby P, Hutchison WD, Lang AE, Lozano AM, Dostrovsky JO (2002) Dependence of subthalamic nucleus oscillations on movement and dopamine in Parkinson’s disease. Brain 125:1196–1209

    Article  PubMed  Google Scholar 

  • Llinás RR, Ribary U, Jeanmonod D, Kronberg E, Mitra PP (1999) Thalamocortical dysrhythmia: a neurological and neuropsychiatric syndrome characterized by magnetoencephalography. Proc Natl Acad Sci USA 96:15222–15227

    Article  PubMed  Google Scholar 

  • Lopes da Silva F (1991) Neural mechanisms underlying brain waves: from neural membranes to networks. Electroencephalogr Clin Neurophysiol 79:81–93

    Article  PubMed  CAS  Google Scholar 

  • Matelli M, Rizzolatti G, Bettinardi V, Gilardi MC, Perani D, Rizzo G, Fazio F (1993) Activation of precentral and mesial motor areas during the execution of elementary proximal and distal arm movements: a PET study. NeuroReport 4:1295–1298

    Article  PubMed  CAS  Google Scholar 

  • Marsden CD, Obeso JA (1994) The functions of the basal ganglia and the paradox of stereotaxic surgery in Parkinson’s disease. Brain 117:877–897

    Article  PubMed  Google Scholar 

  • Marsden JF, Ashby P, Limousin-Dowsey P, Rothwell JC, Brown P (2000) Coherence between cerebellar thalamus, cortex and muscle in man. Cerebellar thalamus interactions. Brain 123:1459–1470

    Article  PubMed  Google Scholar 

  • Marsden JF, Limousin-Dowsey P, Ashby P, Pollak P, Brown P (2001) Subthalamic nucleus, sensorimotor cortex and muscle interrelationships in Parkinson’s Disease. Brain 124:378–388

    Article  PubMed  CAS  Google Scholar 

  • Neuper C, Pfurtscheller G (2001) Evidence for distinct beta resonance frequencies in human EEG related to specific sensorimotor cortical areas. Clin Neurophysiol 112:2084–2097

    Article  PubMed  CAS  Google Scholar 

  • Niedermeyer E (1999) The normal EEG of the waking adult. In: Niedermeyer E, Lopes da Silva F (eds) Electroencephalography. Basic principles, clinical applications and related fields, 4th edn. Williams and Wilkins, Baltimore, pp 149–173

    Google Scholar 

  • Ohye C (2000) Use of selective thalamotomy for various kinds of movement disorder, based on basic studies. Stereotact Funct Neurosurg 75:54–65

    Article  PubMed  CAS  Google Scholar 

  • Paradiso G, Cunic D, Saint-Cyr JA, Hoque T, Lozano AM, Lang AE, Chen R (2004) Involvement of human thalamus in the preparation of self-paced movement. Brain 127:2717–2731

    Article  PubMed  Google Scholar 

  • Paus T (2002) Combination of transcranial magnetic stimulation with brain imaging. In: Mazziotta J, Toga A (eds) Brain mapping: the methods, 2nd edn. Academic, San Diego, pp 691–705

    Google Scholar 

  • Paus T (2003) Principles of functional neuroimaging. In: Schiffer RB, Rao SM, Fogel BS (eds) Neuropsychiatry, 2 edn. Lippincott, Williams and Wilkins, pp 63–90

  • Paus T, Petrides M, Evans AC, Meyer E (1993) Role of the human anterior cingulate cortex in the control of occulomotor, manual, and speech responses: a positron emission tomography study. J Neurophysiol 70:453–469

    PubMed  CAS  Google Scholar 

  • Paus T, Jech R, Thompson CJ, Comeau R, Peters T, Evans AC (1997) Transcranial magnetic stimulation during positron emission tomography: a new method of studying connectivity of the human cerebral cortex. J Neurosci 17:3178–3184

    PubMed  CAS  Google Scholar 

  • Paus T, Sipila PK, Strafella AP (2001) Synchronization of neuronal activity in the human sensorimotor cortex by transcranial magnetic stimulation: a combined TMS/EEG study. J Neurophysiol 86:1983–1990

    PubMed  CAS  Google Scholar 

  • Pfurtscheller G, Woertz M, Supp G, Lopes da Silva FH (2003) Early onset of post-movement beta electroencephalogram synchronization in the supplementary motor area during self-paced finger movement in man. Neurosci Lett 339:111–114

    Article  PubMed  CAS  Google Scholar 

  • Pierantozzi M, Palmieria MG, Mazzone P, Marciania MG, Rossini PM, Stefani A, Giacomini P, Peppe A, Stanzione P (2002) Deep brain stimulation of both subthalamic nucleus and internal globus pallidus restores intracortical inhibition in Parkinson’s disease paralleling apomorphine effects: a paired magnetic stimulation study. Clin Neurophysiol 113:108–113

    Article  PubMed  CAS  Google Scholar 

  • Priori A, Foffani G, Pesenti A, Bianchi A, Chiesa V, Baselli G, Caputo E, Tamma F, Rampini P, Egidi M, Locatelli Barbieri S, Scarlato G (2002) Neurol Sci 23:S101–S102

    Article  PubMed  Google Scholar 

  • Priori A, Foffani G, Pesenti A, Tamma F, Bianchi AM, Pellegrini M, Locatelli M, Moxon KA, Villani RM (2004) Exp Neurol 189:369–379

    Article  PubMed  CAS  Google Scholar 

  • Rouiller EM, Liang F, Babalian A, Moret V, Wiesendanger M (1994) Cerebellothalamocortical and pallidothalamocortical projections to the primary and supplementary motor cortical areas: a multiple tracing study in macaque monkeys. J Comp Neurol 345:185–213

    Article  PubMed  CAS  Google Scholar 

  • Sarnthein J, Morel A, Von Stein A, Jeanmonod D (2003) Thalamic theta field potentials and EEG: high thalamocortical coherence in patients with neurogenic pain, epilepsy and movement disorders. Thalamus Related Syst 2:231–238

    Google Scholar 

  • Schaltenbrand G, Wahren W (1977) Atlas of stereotaxy of the human brain. Thieme, Stuttgart

    Google Scholar 

  • Schlaug G, Knorr U, Seitz R (1994) Inter-subject variability of cerebral activations in acquiring motor skill: a study with positron emission tomography. Exp Brain Res 98:523–534

    Article  PubMed  CAS  Google Scholar 

  • Siebner HR, Rossmeier C, Mentschel C, Peinemann A, Conrad B (2000) Short-term motor improvement after sub-threshold 5-Hz repetitive tanscranial magnetic stimulation of the primary motor hand area in Parkinson’s disease. J Neurol Sci 178:91–94

    Article  PubMed  CAS  Google Scholar 

  • Soikkeli R, Partanen J, Soininen H, Pääkkönen A, Riekkinen P Sr (1991) Slowing of EEG in Parkinson’s disease. Electroencephalogr Clin Neurophysiol 79:159–165

    Article  PubMed  CAS  Google Scholar 

  • Steriade M (1999) Cellular substrates of brain rhythms. In: Niedermeyer E, Lopes da Silva F (eds) Electroencephalography. Basic principles, clinical applications and related fields, 4th edn. Williams and Wilkins, Baltimore, pp 28–75

  • St-Jean P, Sadikot AF, Collins L, Clonda D, Kasrai R, Evans AC, Peters TM (1998) Automated atlas integration and interactive three-dimensional visualization tools for planning and guidance in functional neurosurgery. IEEE Trans Med Imaging 17:672–680

    Article  PubMed  CAS  Google Scholar 

  • Talairach J, Tournoux P (1988) Co-planar stereotactic atlas of the human brain: dimensional proportional system: an approach to cerebral imaging. Thieme, Stuttgart, Germany

  • Van Der Werf YD, Paus T (2006) The neural response to transcranial magnetic stimulation of the human motor cortex. I. Intracortical and cortico-cortical contributions. DOI 10.1007/s00221-006-0551-2

  • Virtanen J, Ruohonen J, Naatanen R, Ilmoniemi RJ (1999) Instrumentation for the measurement of electric brain responses to transcranial magnetic stimulation. Med Biol Eng Comput 37:332–326

    Article  Google Scholar 

  • Williams D, Tijssen M, Van Bruggen G, Bosch A, Insola A, Di Lazzaro V, Mazzone P, Oliviero A, Quartarone A, Speelman H, Brown P (2002). Dopamine-dependent changes in the functional connectivity between basal ganglia and cerebral cortex in humans. Brain 125:1558–1569

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ysbrand D. Van Der Werf.

Additional information

The first author was funded by a fellowship from the Canadian Institute of Health Research (CIHR).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Van Der Werf, Y.D., Sadikot, A.F., Strafella, A.P. et al. The neural response to transcranial magnetic stimulation of the human motor cortex. II. Thalamocortical contributions. Exp Brain Res 175, 246–255 (2006). https://doi.org/10.1007/s00221-006-0548-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-006-0548-x

Keywords

Navigation